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Motor cortical dynamics are shaped by multiple distinct subspaces during naturalistic behavior

View ORCID ProfileMatthew G. Perich, Sara Conti, Marion Badi, View ORCID ProfileAndrew Bogaard, Beatrice Barra, View ORCID ProfileSophie Wurth, View ORCID ProfileJocelyne Bloch, View ORCID ProfileGregoire Courtine, View ORCID ProfileSilvestro Micera, View ORCID ProfileMarco Capogrosso, View ORCID ProfileTomislav Milekovic
doi: https://doi.org/10.1101/2020.07.30.228767
Matthew G. Perich
1Department of Fundamental Neuroscience, University of Geneva, Geneva, Switzerland
2Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, USA
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  • For correspondence: mperich@gmail.com
Sara Conti
3Department of Medicine, University of Fribourg, Fribourg, Switzerland
4The BioRobotics Institute and Department of Excellent in Robotics and AI, Scuola Superiore Sant’Anna, Pisa, Italy
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Marion Badi
5Bertarelli Foundation Chair in Translational Neuroengineering, Center for Neuroprosthetics and Institute of Bioengineering, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland
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Andrew Bogaard
5Bertarelli Foundation Chair in Translational Neuroengineering, Center for Neuroprosthetics and Institute of Bioengineering, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland
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Beatrice Barra
3Department of Medicine, University of Fribourg, Fribourg, Switzerland
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Sophie Wurth
5Bertarelli Foundation Chair in Translational Neuroengineering, Center for Neuroprosthetics and Institute of Bioengineering, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland
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Jocelyne Bloch
6Centre hospitalier universitaire Vaudois (CHUV), Lausanne, Switzerland
7Defitech Center for Interventional Neurotherapies (NeuroRestore), Lausanne, Switzerland
8Center for Neuroprosthetics and the Brain Mind Institute, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland
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Gregoire Courtine
6Centre hospitalier universitaire Vaudois (CHUV), Lausanne, Switzerland
7Defitech Center for Interventional Neurotherapies (NeuroRestore), Lausanne, Switzerland
8Center for Neuroprosthetics and the Brain Mind Institute, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland
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Silvestro Micera
4The BioRobotics Institute and Department of Excellent in Robotics and AI, Scuola Superiore Sant’Anna, Pisa, Italy
5Bertarelli Foundation Chair in Translational Neuroengineering, Center for Neuroprosthetics and Institute of Bioengineering, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland
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Marco Capogrosso
3Department of Medicine, University of Fribourg, Fribourg, Switzerland
9Department of Neurological Surgery, University of Pittsburgh, Pittsburgh, PA, USA
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Tomislav Milekovic
1Department of Fundamental Neuroscience, University of Geneva, Geneva, Switzerland
6Centre hospitalier universitaire Vaudois (CHUV), Lausanne, Switzerland
7Defitech Center for Interventional Neurotherapies (NeuroRestore), Lausanne, Switzerland
8Center for Neuroprosthetics and the Brain Mind Institute, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland
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ABSTRACT

Behavior relies on continuous influx of sensory information about the body and the environment. In primates, cortex integrates somatic feedback to accurately reach and manipulate objects. Yet, in many experimental regimes motor cortex seems paradoxically to operate as a feedforward, rather than feedback-driven, system. Here, we recorded simultaneously from motor and somatosensory cortex as monkeys performed a naturalistic reaching and object interaction behavior. We studied how unexpected feedback from behavioral errors influences cortical dynamics. Motor cortex generally exhibited robust feedforward dynamics, yet displayed feedback-driven dynamics surrounding correction of behavioral errors. We then decomposed motor cortical activity into orthogonal subspaces capturing communication with somatosensory cortex or behavior-generating dynamics. During error correction, the communication subspace became feedback-driven, while the behavioral subspace maintained feedforward dynamics. We therefore demonstrate that cortical activity is compartmentalized within distinct subspaces that shape the population dynamics, enabling flexible integration of salient inputs with ongoing activity for robust behavior.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵* these authors jointly supervised this work

  • Updated PDF to include a missing block of text in the results.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted August 03, 2020.
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Motor cortical dynamics are shaped by multiple distinct subspaces during naturalistic behavior
Matthew G. Perich, Sara Conti, Marion Badi, Andrew Bogaard, Beatrice Barra, Sophie Wurth, Jocelyne Bloch, Gregoire Courtine, Silvestro Micera, Marco Capogrosso, Tomislav Milekovic
bioRxiv 2020.07.30.228767; doi: https://doi.org/10.1101/2020.07.30.228767
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Motor cortical dynamics are shaped by multiple distinct subspaces during naturalistic behavior
Matthew G. Perich, Sara Conti, Marion Badi, Andrew Bogaard, Beatrice Barra, Sophie Wurth, Jocelyne Bloch, Gregoire Courtine, Silvestro Micera, Marco Capogrosso, Tomislav Milekovic
bioRxiv 2020.07.30.228767; doi: https://doi.org/10.1101/2020.07.30.228767

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